The genus Xenopus as a multispecies model for evolutionary and comparative immunobiology of the 21st century

Developmental and Comparative Immunology

Volumn 35, Issue 9, 2011, Pages 916-923

  Robert, Jacques ^a   Cohen, Nicholas ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Genome evolution; Immunogenetics; Nonclassical MHC class I; Tumor immunity

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MONOCLONAL ANTIBODY;

AMPHIBIA; ANGIOGENESIS; CELL LINE; EXPERIMENTAL MODEL; GENE CONTROL; GENE DUPLICATION; GENE MAPPING; GENE SEQUENCE; GENETIC CONSERVATION; GENUS; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOBIOLOGY; IMMUNOLOGICAL TOLERANCE; INBRED STRAIN; INFECTION RESISTANCE; LYMPHANGIOGENESIS; MAJOR HISTOCOMPATIBILITY COMPLEX; MAMMAL; MEDICAL RESEARCH; MOLECULAR CLONING; MUTAGENESIS; NONHUMAN; POLYPLOIDY; PRIORITY JOURNAL; REVIEW; SPECIES DIFFERENCE; TUMOR IMMUNITY; XENOPUS;

AMPHIBIA; MAMMALIA; XENOPODINAE; XENOPUS TROPICALIS;

EID: 79959548093     PISSN: 0145305X     EISSN: 0145305X     Source Type: Journal    
DOI: 10.1016/j.dci.2011.01.014     Document Type: Review

References (94)

1. Bechtold T.E., Smith P.B., Turpen J.B. Differential stem cell contributions to thymocyte succession during development of Xenopus laevis. J. Immunol. 1992, 148(10):2975-2982.
2. Beck C.W., Christen B., Slack J.M. Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev. Cell 2003, 5(3):429-439.
3. Beck C.W., Christen B., Barker D., Slack J.M. Temporal requirement for bone morphogenetic proteins in regeneration of the tail and limb of Xenopus tadpoles. Mech. Dev. 2006, 123(9):674-688.
4. Beck C.W., Izpisua Belmonte J.C., Christen B. Beyond early development: Xenopus as an emerging model for the study of regenerative mechanisms. Dev. Dyn. 2009, 238(6):1226-1248.
5. Bottaro A., Inlay M.A., Matzke N.J. Immunology in the spotlight at the Dover 'Intelligent Design' trial. Nat. Immunol. 2006, 7(5):433-435.
6. Braaten D.C., McClellan J.S., Messaoudi I., Tibbetts S.A., McClellan K.B., Nikolich-Zugich J., et al. Effective control of chronic gamma-herpesvirus infection by unconventional MHC class Ia-independent CD8 T cells. PLoS Pathog. 2006, 2(5):e37.
7. Briggs R., King T.J. Transplantation of living nuclei from blastula cells into enucleated frogs' eggs. Proc. Natl. Acad. Sci. U. S. A. 1952, 38(5):455-463.
8. Carey C., Cohen N., Rollins-Smith L. Amphibian declines: an immunological perspective. Dev. Comp. Immunol. 1999, 23(6):459-472.
9. Chardonnens X., Du Pasquier L. Induction of skin allograft tolerance during metamorphosis of the toad Xenopus laevis: a possible model for studying generation of self tolerance to histocompatibility antigens. Eur. J. Immunol. 1973, 3(9):569-573.
10. Chen Y., Costa R.M., Love N.R., Soto X., Roth M., Paredes R., et al. C/EBPalpha initiates primitive myelopoiesis in pluripotent embryonic cells. Blood 2009, 114(1):40-48.
11. Chesneau A., Sachs L.M., Chai N., Chen Y., Du Pasquier L., Loeber J., et al. Transgenesis procedures in Xenopus. Biol. Cell 2008, 100(9):503-521.
12. Chida S., Goyos A., Robert J. Phylogeny and developmental expression of CD8alpha, beta and CD4 genes in the amphibian Xenopus. Dev. Comp. Immunol. 2010, 35(3):366-377.
13. Chinchar V.G., Hyatt A., Miyazaki T., Williams T. Family Iridoviridae: poor viral relations no longer. Curr. Top. Microbiol. Immunol. 2009, 328123-328170.
14. Costa R.M., Soto X., Chen Y., Zorn A.M., Amaya E. spib is required for primitive myeloid development in Xenopus. Blood 2008, 112(6):2287-2296.
15. Courtet M., Flajnik M., Du Pasquier L. Major histocompatibility complex and immunoglobulin loci visualized by in situ hybridization on Xenopus chromosomes. Dev. Comp. Immunol. 2001, 25(2):149-157.
16. Dahmane N., Lee J., Robins P., Heller P., Ruiz i Altaba A. Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours. Nature 1997, 389(6653):876-881.
17. DiMarzo S.J., Cohen N. Immunogenetic aspects of in vivo allotolerance induction during the ontogeny of Xenopus laevis. Immunogenetics 1982, 16(2):103-116.
18. DiMarzo S.J., Cohen N. An in vivo study of the ontogeny of alloreactivity in the frog, Xenopus laevis. Immunology 1982, 45(1):39-48.
19. Du Pasquier L., Courtney Smith L. Workshop report: evolutionary immunobiology-new approaches, new paradigms. Dev. Comp. Immunol. 2003, 27(4):263-271.
20. Du Pasquier L., Flajnik M.F. Expression of MHC class II antigens during Xenopus development. Dev. Immunol. 1990, 1(2):85-95.
21. Du Pasquier L., Weiss N. The thymus during the ontogeny of the toad Xenopus laevis: growth, membrane-bound immunoglobulins and mixed lymphocyte reaction. Eur. J. Immunol. 1973, 3(12):773-777.
22. Du Pasquier L., Schwager J., Flajnik M.F. The immune system of Xenopus. Annu. Rev. Immunol. 1989, 7251-7275.
23. Du Pasquier L., Wilson M., Sammut B. The fate of duplicated immunity genes in the dodecaploid Xenopus ruwenzoriensis. Front. Biosci. 2009, 14177-14191.
24. Dunn G.P., Old L.J., Schreiber R.D. The three Es of cancer immunoediting. Annu. Rev. Immunol. 2004, 22329-22360.
25. Evans B.J. Genome evolution and speciation genetics of clawed frogs (Xenopus and Silurana). Front. Biosci. 2008, 134687-134706.
26. Evans B.J., Kelley D.B., Melnick D.J., Cannatella D.C. Evolution of RAG-1 in polyploid clawed frogs. Mol. Biol. Evol. 2005, 22(5):1193-1207.
27. Fisher M.C., Garner T.W., Walker S.F. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu. Rev. Microbiol. 2009, 63291-63310.
28. Flajnik M.F., Du Pasquier L. MHC class I antigens as surface markers of adult erythrocytes during the metamorphosis of Xenopus. Dev. Biol. 1988, 128(1):198-206.
29. Flajnik M.F., Kasahara M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 2010, 11(1):47-59.
30. Flajnik M.F., Hsu E., Kaufman J.F., Pasquier L.D. Changes in the immune system during metamorphosis of Xenopus. Immunol. Today 1987, 8(2):58-64.
31. Flajnik M.F., Kasahara M., Shum B.P., Salter-Cid L., Taylor E., Du Pasquier L. A novel type of class I gene organization in vertebrates: a large family of non-MHC-linked class I genes is expressed at the RNA level in the amphibian Xenopus. EMBO J. 1993, 12(11):4385-4396.
32. Fukazawa T., Naora Y., Kunieda T., Kubo T. Suppression of the immune response potentiates tadpole tail regeneration during the refractory period. Development 2009, 136(14):2323-2327.
33. Gilbert S.F. Opening Darwin's black box: teaching evolution through developmental genetics. Nat. Rev. Genet. 2003, 4(9):735-741.
34. Goyos A., Robert J. Tumorigenesis and anti-tumor immune responses in Xenopus. Front. Biosci. 2009, 14167-14176.
35. Goyos A., Cohen N., Gantress J., Robert J. Anti-tumor MHC class Ia-unrestricted CD8 T cell cytotoxicity elicited by the heat shock protein gp96. Eur. J. Immunol. 2004, 34(9):2449-2458.
36. Goyos A., Guselnikov S., Chida A.S., Sniderhan L.F., Maggirwar S.B., Nedelkovska H., et al. Involvement of nonclassical MHC class Ib molecules in heat shock protein-mediated anti-tumor responses. Eur. J. Immunol. 2007, 37(6):1494-1501.
37. Goyos A., Ohta Y., Guselnikov S., Robert J. Novel nonclassical MHC class Ib genes associated with CD8 T cell development and thymic tumors. Mol. Immunol. 2009, 46(8-9):1775-1786.
38. Goyos A., Sowa J., Ohta Y., Robert J. Genomic organization, expression patterns and phylogeny of nonclassical MHC class Ib genes in the Xenopus laevis sister species Silurana (Xenopus) tropicalis. J. Immunol. 2010, 186:372-381.
39. Heasman J. Patterning the early Xenopus embryo. Development 2006, 133(7):1205-1217.
40. Hellsten U., Harland R.M., Gilchrist M.J., Hendrix D., Jurka J., Kapitonov V., et al. The genome of the Western clawed frog Xenopus tropicalis. Science 2010, 328(5978):633-636.
41. Hochedlinger K., Jaenisch R. Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 2002, 415(6875):1035-1038.
42. Hochedlinger K., Jaenisch R. Nuclear transplantation: lessons from frogs and mice. Curr. Opin. Cell Biol. 2002, 14(6):741-748.
43. Horton J.D., Horton T.L., Dzialo R., Gravenor I., Minter R., Ritchie P., et al. T-cell and natural killer cell development in thymectomized Xenopus. Immunol. Rev. 1998, 166245-166258.
44. Horton T.L., Stewart R., Cohen N., Rau L., Ritchie P., Watson M.D., et al. Ontogeny of Xenopus NK cells in the absence of MHC class I antigens. Dev. Comp. Immunol. 2003, 27(8):715-726.
45. Jackson J.A., Tinsley R.C. Evolutionary diversity in polystomatids infecting tetraploid and octoploid Xenopus in East African highlands: biological and molecular evidence. Parasitology 2007, 134(Pt 9):1223-1235.
46. Jackson J.A., Pleass R.J., Cable J., Bradley J.E., Tinsley R.C. Heterogeneous interspecific interactions in a host-parasite system. Int. J. Parasitol. 2006, 36(13):1341-1349.
47. Kato Y., Salter-Cid L., Flajnik M.F., Kasahara M., Namikawa C., Sasaki M., et al. Isolation of the Xenopus complement factor B complementary DNA and linkage of the gene to the frog MHC. J. Immunol. 1994, 153(10):4546-4554.
48. Kirak O., Frickel E.M., Grotenbreg G.M., Suh H., Jaenisch R., Ploegh H.L. Transnuclear mice with predefined T cell receptor specificities against Toxoplasma gondii obtained via SCNT. Science 2010, 328(5975):243-248.
49. Kobel H.R., Du Pasquier L. Genetics of polyploid Xenopus. Trends Genet. 1986, 12310-12314.
50. Kroll K.L., Amaya E. Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation. Development 1996, 122(10):3173-3183.
51. Ladi E., Yin X., Chtanova T., Robey E.A. Thymic microenvironments for T cell differentiation and selection. Nat. Immunol. 2006, 7(4):338-343.
52. Mak T.W., Penninger J.M., Ohashi P.S. Knockout mice: a paradigm shift in modern immunology. Nat. Rev. Immunol. 2001, 1(1):11-19.
53. Marr S., Morales H., Bottaro A., Cooper M., Flajnik M., Robert J. Localization and differential expression of activation-induced cytidine deaminase in the amphibian Xenopus upon antigen stimulation and during early development. J. Immunol. 2007, 179(10):6783-6789.
54. McLysaght A., Hokamp K., Wolfe K.H. Extensive genomic duplication during early chordate evolution. Nat. Genet. 2002, 31(2):200-204.
55. Morales H.D., Robert J. Characterization of primary and memory CD8 T-cell responses against ranavirus (FV3) in Xenopus laevis. J. Virol. 2007, 81(5):2240-2248.
56. Mukaigasa K., Hanasaki A., Maeno M., Fujii H., Hayashida S., Itoh M., et al. The keratin-related Ouroboros proteins function as immune antigens mediating tail regression in Xenopus metamorphosis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(43):18309-18314.
57. Nagata S., Cohen N. Specific in vivo and nonspecific in vitro alloreactivities of adult frogs (Xenopus laevis) that were thymectomized during early larval life. Eur. J. Immunol. 1983, 13(7):541-545.
58. Ny A., Koch M., Schneider M., Neven E., Tong R.T., Maity S., et al. A genetic Xenopus laevis tadpole model to study lymphangiogenesis. Nat. Med. 2005, 11(9):998-1004.
59. Ny A., Koch M., Vandevelde W., Schneider M., Fischer C., Diez-Juan A., et al. Role of VEGF-D and VEGFR-3 in developmental lymphangiogenesis, a chemicogenetic study in Xenopus tadpoles. Blood 2008, 112(5):1740-1749.
60. Ohno S. Evolution by Gene Duplication 1970, Springer-Verlag, Berlin/Heidelberg/New York.
61. Ohno S. Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Semin. Cell. Dev. Biol 1999, 10517-10522.
62. Ohta Y., Goetz W., Hossain M.Z., Nonaka M., Flajnik M.F. Ancestral organization of the MHC revealed in the amphibian Xenopus. J. Immunol. 2006, 176(6):3674-3685.
63. Parra Z.E., Ohta Y., Criscitiello M.F., Flajnik M.F., Miller R.D. The dynamic TCRdelta: TCRdelta chains in the amphibian Xenopus tropicalis utilize antibody-like V genes. Eur. J. Immunol. 2010, 40(8):2319-2329.
64. Pollet N., Muncke N., Verbeek B., Li Y., Fenger U., Delius H., et al. An atlas of differential gene expression during early Xenopus embryogenesis. Mech. Dev. 2005, 122(3):365-439.
65. Prince A.L., Yin C.C., Enos M.E., Felices M., Berg L.J. The Tec kinases Itk and Rlk regulate conventional versus innate T-cell development. Immunol. Rev. 2009, 228(1):115-131.
66. Ramsey J.P., Reinert L.K., Harper L.K., Woodhams D.C., Rollins-Smith L.A. Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infect. Immun. 2010, 78(9):3981-3992.
67. Rau L., Gantress J., Bell A., Stewart R., Horton T., Cohen N., et al. Identification and characterization of Xenopus CD8+ T cells expressing an NK cell-associated molecule. Eur. J. Immunol. 2002, 32(6):1574-1583.
68. Robert J., Ohta Y. Comparative and developmental study of the immune system in Xenopus. Dev. Dyn. 2009, 238(6):1249-1270.
69. Robert J., Guiet C., Du Pasquier L. Ontogeny of the alloimmune response against a transplanted tumor in Xenopus laevis. Differentiation 1995, 59(3):135-144.
70. Robert J., Guiet C., Cohen N., Du Pasquier L. Effects of thymectomy and tolerance induction on tumor immunity in adult Xenopus laevis. Int. J. Cancer 1997, 70(3):330-334.
71. Robert J., Menoret A., Basu S., Cohen N., Srivastava P.R. Phylogenetic conservation of the molecular and immunological properties of the chaperones gp96 and hsp70. Eur. J. Immunol. 2001, 31(1):186-195.
72. Robert J., Gantress J., Rau L., Bell A., Cohen N. Minor histocompatibility antigen-specific MHC-restricted CD8 T cell responses elicited by heat shock proteins. J. Immunol. 2002, 168(4):1697-1703.
73. Robert J., Ramanayake T., Maniero G.D., Morales H., Chida A.S. Phylogenetic conservation of glycoprotein 96 ability to interact with CD91 and facilitate antigen cross-presentation. J. Immunol. 2008, 180(5):3176-3182.
74. Robert J., Goyos A., Nedelkovska H. Xenopus, a unique comparative model to explore the role of certain heat shock proteins and non-classical MHC class Ib gene products in immune surveillance. Immunol. Res. 2009, 45:114-122.
75. Rollins-Smith L.A. Metamorphosis and the amphibian immune system. Immunol. Rev. 1998, 166221-166230.
76. Rollins-Smith L.A., Blair P. Expression of class II major histocompatibility complex antigens on adult T cells in Xenopus is metamorphosis-dependent. Dev. Immunol. 1990, 1(2):97-104.
77. Rollins-Smith L.A., Doersam J.K., Longcore J.E., Taylor S.K., Shamblin J.C., Carey C., et al. Antimicrobial peptide defenses against pathogens associated with global amphibian declines. Dev. Comp. Immunol. 2002, 26(1):63-72.
78. Rosenblum E.B., Poorten T.J., Settles M., Murdoch G.K., Robert J., Maddox N., et al. Genome-wide transcriptional response of Silurana (Xenopus) tropicalis to infection with the deadly chytrid fungus. PLoS ONE 2009, 4(8):e6494.
79. Saharinen P., Helotera H., Miettinen J., Norrmen C., D'Amico G., Jeltsch M., et al. Claudin-like protein 24 interacts with the VEGFR-2 and VEGFR-3 pathways and regulates lymphatic vessel development. Genes Dev. 2010, 24(9):875-880.
80. Salter-Cid L., Nonaka M., Flajnik M.F. Expression of MHC class Ia and class Ib during ontogeny: high expression in epithelia and coregulation of class Ia and lmp7 genes. J. Immunol. 1998, 160(6):2853-2861.
81. Saltis M., Criscitiello M.F., Ohta Y., Keefe M., Trede N.S., Goitsuka R., et al. Evolutionarily conserved and divergent regions of the autoimmune regulator (Aire) gene: a comparative analysis. Immunogenetics 2008, 60(2):105-114.
82. Sato K., Flajnik M.F., Du Pasquier L., Katagiri M., Kasahara M. Evolution of the MHC: isolation of class II beta-chain cDNA clones from the amphibian Xenopus laevis. J. Immunol. 1993, 150(7):2831-2843.
83. Semon M., Wolfe K.H. Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(24):8333-8338.
84. Shum B.P., Avila D., Du Pasquier L., Kasahara M., Flajnik M.F. Isolation of a classical MHC class I cDNA from an amphibian. Evidence for only one class I locus in the Xenopus MHC. J. Immunol. 1993, 151(10):5376-5386.
85. Slack J.M., Lin G., Chen Y. The Xenopus tadpole: a new model for regeneration research. Cell. Mol. Life Sci. 2008, 65(1):54-63.
86. Suzuki M., Takamura Y., Maeno M., Tochinai S., Iyaguchi D., Tanaka I., et al. Xenopus laevis macrophage migration inhibitory factor is essential for axis formation and neural development. J. Biol. Chem. 2004, 279(20):21406-21414.
87. Tinsley R.C., Kobel H.R. The Biology of Xenopus 1996, Oxford University Press, USA.
88. Turpen J.B., Smith P.B. Location of hemopoietic stem cells influences frequency of lymphoid engraftment in Xenopus embryos. J. Immunol. 1989, 143(11):3455-3460.
89. Vize P.D., Vaughan A., Krieg P. Expression of the N-myc proto-oncogene during the early development of Xenopus laevis. Development 1990, 110(3):885-896.
90. Wabl M.R., Brun R.B., Du Pasquier L. Lymphocytes of the toad Xenopus laevis have the gene set for promoting tadpole development. Science 1975, 190(4221):1310-1312.
91. Wallingford J.B. Tumors in tadpoles: the Xenopus embryo as a model system for the study of tumorigenesis. Trends Genet. 1999, 15(10):385-388.
92. Warr G.W., Chapman R.W., Smith L.C. Evolutionary immunobiology: new approaches, new paradigms. Dev. Comp. Immunol. 2003, 27(4):257-262.
93. Yang S., Lockwood A., Hollett P., Ford R., Kao K. Overexpression of a novel Xenopus rel mRNA gene induces tumors in early embryos. J. Biol. Chem. 1998, 273(22):13746-13752.
94. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415(6870):389-395.